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Vol. 13(1), pp. 35-40, January-June 2021 DOI: 10.5897/JPVB2020.0380 Article Number: 97546A566120 ISSN: 2141-2510 Copyright ©2021 Author(s) retain the copyright of this article Journal of Parasitology and Vector Biology http://www.academicjournals.org/JPVB

Full Length Research Paper

Prevalence of soil-transmitted helminthiasis among primary school pupils in Ipogun, Ondo State, Nigeria

Mobolanle Oladipo Oniya1 and Oluwasegun John Jegede1,2*

1Parasitology, Environmental Biology and Public Health Unit, Department of Biology, School of Sciences, The Federal University of Technology, P. M. B 704, Akure, Ondo State, Nigeria. 2Disease Surveillance and Notification Unit, Primary Health Care Authority, Ondo State Ministry of Health, Akure, Nigeria.

Received 20 January, 2020; Accepted 19 March, 2020

The prevalence of Soil-Transmitted Helminthiasis (STH) was investigated among pupils of three selected primary schools in Ipogun, Ifedore Local Government Area of Ondo State, Nigeria. A total of 298 stool samples were collected from pupils across schools and examined for eggs of Soil- Transmitted Helminths (STHs) using concentration method. Results showed that 190 (63.8%) of the 298 pupils were positive for STHs. Ascaris lumbricoides was the most prevalent (25.5%) parasite in the pupils (n = 76), followed by Strongyloides stercoralis, 19.8% (n = 59) and hookworm, 17.8% (n = 53). Trichuris trichiura had the least prevalence of 0.7% (n = 2). Single infestation in the pupils accounted for 160 (84.2%) cases. Of the schools visited, the highest prevalence (74.2%) was recorded in Muslim Nursery and Primary School, followed by St. Jude (70.0%) and Morohunkeji Nursery and Primary School (50.0%). Statistically, there was a significantly lower (P ≤ 0.05) prevalence of STHs in Morohunkeji School compared to the other schools in the study area. The prevalence (50.0%) recorded in both male and female pupils was the same (n = 95) while the prevalence of single infestation in the male pupils was 50.6% (n = 81), higher than that of female pupils, 49.4% (n = 79). The occurrence of co-infestation (or double infestation) in the female pupils was 53.3% (n = 16), higher than that of the male pupils, 46.7% (n = 14). The prevalence recorded across gender and statuses of infestation were statistically insignificant (P > 0.05). As a result of helminth infestation, there is need for routine deworming exercises for school-aged children, maintaining good environmental sanitation, as well as health educating of village dwellers in rural communities for effective control of STH in endemic communities.

Key words: Helminthiasis, prevalence, soil infestation, school pupils, concentration method.

INTRODUCTION

Soil-Transmitted Helminths (STHs) are a group of soil contaminated with faecal matter containing the nematodes (parasitic) worms that afflict humans of eggs/larvae of the parasites, foodstuffs and/or water infective eggs or contact with larvae. STHs exhibit life supplies (Chhabra and Singla, 2009). The morbidity cycles that involve no intermediate host or vector (direct caused by STHs is most commonly associated with life cycle). They infect many animals and humans through infestations of moderate to heavy intensity (Neva and

*Corresponding author. E-mail: [email protected]. Tel: +2347061683686.

Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution License 4.0 International License 36 J. Parasitol. Vector Biol.

Brown, 1994; Nokes and Bundy, 1994). (SDGs). It is on these premises that the goal of this Previous research revealed that the main STHs which research work was established to assess the prevalence cause common clinical disorders in man are Ascaris of STH infestation among primary school pupils (school- lumbricoides (the large roundworm, which causes aged children) in the study area. Ascariasis), Trichuris trichiura (the whipworm, which causes Trichuriasis), and the blood-feeding hookworms (Ancylostoma duodenale and Necator americanus) which MATERIALS AND METHODS cause Ancylostomiasis. There is another species that infect humans; Strongyloides stercoralis which causes Study area

Strongyloidiasis (Bethony et al., 2006). Recent estimates The study was carried out between January and September of of global prevalence suggest that A. lumbricoides infects 2012 in Ipogun (7° 191 N, 5° 51 E), a town in Ifedore Local 800 million people, while T. trichiura and hookworms Government Area of Ondo State, Southwestern part of Nigeria. The infect 600 million in sub-Saharan Africa, and majority of village is about 14 km away from Akure, the capital city of Ondo people infected were from Nigeria (Ogbe et al., 2002; State, and lies in the rainforest belt of Nigeria. The language of Hotez et al., 2009; Hotez et al., 2012). This significantly communication among dwellers is largely Yoruba. The occupation largely practiced by the majority of village inhabitants is farming with indicates the severity of public health risk among the cocoa being the major product, while other dwellers engaged people. themselves in various businesses (trading), and other self- Remarkably, factors including poverty, poor sanitation, employed occupational practices such as artisanship, privately- inadequate hygiene, illiteracy, ecosystem differences and owned enterprise; and as state civil service employees. There is a overcrowding are directly associated with the infestations stream called “Aponmu” in the village which serves as a major arising from the burden of STHs (Crompton, 1999). STH, source of water for domestic and recreational activities due to the inadequacy of potable pipe and borehole sources of water. traditionally endemic in rural areas, are increasingly becoming a public health concern in urban slums of cities present in tropical and sub-tropical developing countries Study design of the world (Bundy et al., 1988; Pullan and Brooker, 2012). The major endemic regions include Southern and Informed consent and ethical issues

Southwestern China, Southern India, Southeast Asia, Ethical consent and permission was obtained from the Ondo State Sub-Saharan Africa; Central and South America (de Silva Ministry of Health, Akure; village head of Ipogun community, and et al., 2003). As established in the findings of this study, schools head and teachers in the village before embarking on the Savioli et al. (2002) had previously reported that school collection of faecal samples. children are more vulnerable to infestation because of their hygiene and play habits. Moreover, in 2006, it was Collection of stool samples estimated that there were 181 million school-aged children in Sub-Saharan Africa out of which 89 million The pupils of Nursery and Primary schools in Ipogun were recruited were infested with one or more parasitic worms (Hotez for the collection of samples. The subjects in the schools located in and Kamath, 2009). Infections arising from STHs among the community were randomly selected for the study. Faecal school-aged children result in malnutrition, intellectual samples were collected from 298 pupils in Saint (St.) Jude‟s, retardation, as well as cognitive and educational deficits Muslim and Morohunkeji Nursery and Primary schools respectively. All pupils in the schools were screened based on their class (WHO, 2005). Profoundly, such infections have insightful registers and their demographic data were documented. The effects on school performance, attendance and future distribution of well labeled, cleaned, and transparent plastic economic productivity of infected children (Bleakly, 2003; containers with tight-fitting lid was done with the aid of the class Miguel and Kremer, 2003). Also, infestations with STHs register. Instructions were given on how to introduce stool samples may increase the hosts‟ susceptibility to other important into the containers. After the stool collection exercise, the plastic containers with faecal samples were recovered and transported to illnesses, such as malaria, tuberculosis and HIV infection the Postgraduate Research Laboratory (PRL) of the Parasitology (Fincham et al., 2003; Le-Hesran et al., 2004). and Public Health Unit, Department of Biology, Federal University of In addition, hookworm infestations cause pathological Technology Akure, Nigeria; where they were analyzed for STHs. blood loss leading pregnant women and their foetus (offspring) to a higher risk of death during pregnancy and delivery (Drake and Bundy, 2001). In most STHs Laboratory analysis endemic areas, school-aged children suffer the greatest The concentration method (Cheesbrough, 1992, 2000; Gupta and burden; hence, due attention is focused on the health of Singla, 2012) was used to concentrate helminths eggs in 1 g of school children (WHO, 1995). If proper and prompt stool samples (human faeces) in the postgraduate research medical attention is not devoted to curbing STH among laboratory. The 1 g of stool sample collected was placed into a school-aged children, infections with STHs can thwart the small plastic container and mixed with 10 ml of normal saline using effort of a country to provide basic education for her an applicator stick to form a suspension. The suspension was vigorously mixed until the faeces were completely emulsified. It was children (Partnership for Child Development, 1997; then filtered with muslin cloth into another clean plastic container. Girum, 2005) thereby working against the realization of The filtrate was then poured into a test tube to make 10 ml and the United Nations Sustainable Development Goals centrifuged at 2,000 revolutions per minute (rpm) for 3 min. After Oniya and Jegede 37

Table 1. Prevalence of parasites in the examined pupils.

Parasite species Positive (%) Single Infestation (%) Co-Infestation (%) Ascaris lumbricoides 76 (25.5) 70 (43.7) 6 (20.0) Hookworms 53 (17.8) 42 (26.3) 11 (36.7) Strongyloides stercoralis 59 (19.8) 48 (30.0) 11 (36.7) Trichuris trichiura 2 (0.7) - 2 (6.6) Total prevalence (%) 190 (63.8) 160 (100.0) 30 (100.0)

P ≤ 0.05.

Table 2. Prevalence of soil-transmitted helminthiasis among primary school pupils in the study area.

Schools Number examined (%) Male (%) Female (%) Number positive (%) Significance Morohunkeji 104 (34.9) 48 (46.2) 56 (53.9) 52 (50.0) P ≤ 0.05 Muslim 66 (22.2) 35 (53.0) 31 (47.0) 49 (74.2) P > 0.05 St. Jude 128 (42.9) 69 (53.9) 59 (46.0) 89 (70.0) P > 0.05 Total (%) 298 (100.0) 152 (51.0) 146 (49.0) 190 (63.8)

centrifugation, the tubes were removed and the supernatant was trichiura. The prevalence of these worms was decanted. About 3 – 4 ml of 10% formol solution was added to the significantly different in this population (P ≤ 0.05). deposit to form a homogenous suspension and the mixture was Out of the schools examined, Muslim Primary School allowed to stand for 5 min lengthwise. A 3 – 4 ml of diethyl ether was added, shaken vigorously and allowed to stand for 2 min, after had the least examined pupils (male = 35 and female = which it was then centrifuged at 1,000 rpm for 1 min. The faecal 31) but had the highest prevalence of 74.2% (n = 49). debris from the slide of the tube was detached with the aid of a Saint Jude Primary School had the highest examined glass rod (spatula) and the supernatant was discarded while pupils (male = 69 and female = 59) and prevalence was leaving the deposit at the bottom of the centrifuge tube. The deposit 70.0% (n = 89) out of the 128 pupils that were examined. was tapped with finger to mix and using a Pasteur pipette, a drop of the deposit was smeared on a clean, grease-free microscope slide No significant difference (P > 0.05) was recorded for mixed with Lugol‟s iodine, covered with a cover slip and examined prevalence of STHs for both aforementioned schools. using x10 objective lens while the x40 objective lens was used for Morohunkeji Nursery and Primary School had 104 pupils the identification of parasite eggs (WHO, 1991; Cheesbrough, examined, that is, male (n = 48) and female (n = 56) but 1992). As reported by King and Mascie-Taylor (2004), diagnosing showed the least prevalence of 50.0% (n = 52) (Table 2). soil-transmitted parasites is made possible by identifying their eggs This is statistically significant (P ≤ 0.05) from both and larvae microscopically in the sampled stool of infected persons. examined schools above. As observed in Table 3, total examined male pupils Statistical analysis were 152 (51.0%) while examined female pupils were 146 (49.0%). Surprisingly, both male and female pupils All statistical data obtained were subjected to analysis using shared the same prevalence of 50.0% (n = 95). Statistical Package for Social Scientists (SPSS) for windows Interestingly, the prevalence of male pupils (50.6%) with version 21.0. Test of Significance on prevalence of each Soil- single parasitic infestation was greater than that of the Transmitted Helminthic infections among subgroup of positive subjects were determined using the Least Significant Difference female pupils (49.4%) while the prevalence rate (53.3%) (LSD). Statistical differences were assigned at P ≤ 0.05. The mean of female pupils (n = 16) with co-infestation was greater difference is significant at the 0.05 level. than that of the male pupils examined (46.7%) (Figure 1). However, significant difference did not exist between prevalence recorded for both genders (P > 0.05). RESULTS

Out of the total 298 pupils examined from the schools in DISCUSSION the study area, 63.8% (n = 190) were found to be positively infested with one of the parasites listed in Table The prevalence of A. lumbricoides (25.5%), S. stercoralis 1. A. lumbricoides had the highest prevalence of 25.5% (19.8%), hookworm (17.8%), and T. trichiura (0.7%) were (n = 76), followed by S. stercoralis with prevalence of revealed among pupils of three primary schools in the 19.8% (n = 59), hookworm had 17.8% (n = 53) and the research study area. These findings were in agreement least prevalence rate of 0.7% (n = 2) was recorded for T. with the work of Eke et al. (2015) who reported that the 38 J. Parasitol. Vector Biol.

Table 3. Prevalence of soil-transmitted helminthiasis in the study area based on sex.

Sex of pupil Number examined (%) Number infected (%) Male 152 (51.0) 95 (50.0) Female 146 (49.0) 95 (50.0) Total (%) 298 (100.0) 190 (63.8)

P > 0.05.

Figure 1. Prevalence of STH parasites based on infestation status of gender (P > 0.05).

prevalence of these four geohelminths (26.46, 9.58, among the three schools based on the number of 22.50, and 8.54% respectively) were confirmed in the examined pupils, though the school had the least number stool samples of school children of four selected primary of examined pupils (n = 66), leaving only 17 pupils schools in Panda Development Area, Karu Local negative of STH parasites. The main reason for this may Government Area, Nasarawa State, Nigeria. be due to the insanitary environment of the school and In the current research, the overall prevalence of STH her proximity to the refuse, wastes and garbage dumping among the school pupils was high (63.8%, n = 190) as sites, where some of the school pupils defecate. more than half of the total number of population Moreover, refuse dumps are open dumping grounds examined (n = 298) suffered from the parasitic infestation where people defecate and that contaminate the soil with of soil-transmitted helminths either as single infestation or eggs/larvae of STHs through run-offs during flooding of co-infestation. The high rate of prevalence recorded in rain, thereby predisposing parasites into the environment the study area may be due to factors like improper faecal (Ogbolu et al., 2011; Chacha et al., 2013), and thus disposal, poor standard of hygienic living and behaviour; prone individuals susceptible to the high risk of STHs inadequate potable, clean, safe and drinkable source of infestations. The pupils during break or leisure periods water and general poor sanitation culture employed by were often seen playing bare-footed with soil close to the the majority of village dwellers, which were all waste dumped sites and even go sometimes to the characteristics of a rural area where previous researches Aponmu River to play and thereafter, probably eat have shown the infestation by soil-transmitted helminths without washing their hands. When faeces are not to be endemic (Crompton, 1999; Pullan et al., 2014). properly disposed, they may be washed into nearby Pupils from Muslim primary school (n = 49) were shown streams where people frequently visit to meet their to be the most prevalent (74.2%) for STH parasites needs. Some of the pupils also walk bare footed on Oniya and Jegede 39

infected and contaminated soil during school periods or parents of pupils should be willing to allow their wards to even at home, making them prone/exposed to larvae of participate actively in deworming exercises been carried parasites, that penetrate into their body, for example out in schools by both governmental and non– hookworm larvae. It has been posited by Uga et al. governmental agencies, or endeavour to deworm their (1997) that soil contamination status is the most direct children quarterly (4 times in a year). Finally, government link to risk for STHs infections. Furthermore, the findings (executive, judiciary and legislature) must encourage that in this present study is similar with past research works those without toilet facilities in their homes should make that reported high contamination rate of STHs in soil use of publicly-provided toilet facilities or find possible samples of Abuja and Ibadan, Nigeria; respectively in means of constructing one for their personal use. The 2011 (Mohammed et al., 2011; Ogbolu et al., 2011). security agencies should lawfully implement the Prevalence of Soil-Transmitted Helminthiasis in the Executive Order 009 Bill signed into law by the President study area based on sex revealed equal prevalence rate of the Federal Republic of Nigeria on open defecation. (50.0%) for pupils of both genders (male and female) This will help eradicate open defecation which is largely (each has n = 95) infected with STHs parasites. This is in practiced in the area and environs. contrary to the findings of Eke et al. (2015) who reported that in the examined stool samples of school children of four selected primary schools in Panda Development CONFLICT OF INTERESTS Area, Karu Local Government Area, Nasarawa State, Nigeria; male had the highest infection rate of 167 The authors have not declared any conflict of interests. (64.33%) while 155 (70.45%) was recorded in female (P > 0.05). Accordingly, female pupils (n = 16) had more co- infestations (53.3%) as compared to the male pupils (n = ACKNOWLEDGEMENTS 14; 46.7%). The male pupils also were recorded to have higher prevalence rate (50.6%) of single parasitic The authors warmly appreciate the moral backing of the infestation (n = 81) as compared to the female pupils (n = Ondo State Ministry of Health and Schools‟ heads for the 79; 49.4%). Irregular deworming by the pupils may be a ethical clearance and informed consent granted to carry contributive factor towards the observed high prevalence out this research. The cooperation of the school pupils rate. Co-existence of parasites is mostly dependent on and their parents is also valued. the epidemiological factors with similar mode of transmission. Where low unhygienic behaviour thrives, nursery and primary pupils who are weak REFERENCES immunologically are more likely to have helminthiasis Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A (2006). 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